An annotated checklist of Coccinellidae with four new records from Pakistan (Coleoptera, Coccinellidae).

Some new ladybird (Coleoptera: Coccinellidae) records collected during the last four years across Sindh are reported. A first preliminary checklist of ladybirds from Sindh is presented, consisting of one subfamily, ten tribes, 21 genera, and 29 species including four new records, namely Bulaealichatschovii (Hummel), Exochomuspubescens Küster, Scymnus (Pullus) latemaculatus Motschulsky, Scymnus (Pullus) syriacus Marseul, and four varieties of the species Cheilomenessexmaculatus (Fabricius).

Introduction

According to the most recent classification, the family comprises two subfamilies: Leng, 1920 and Latreille, 1807 (sensu Slipinski 2007) based on phylogenetic results (Seago et al. 2011). These changes impact the status of various traditionally recognized tribes and subfamilies, as the onlysubfamilies now recognized are and (Canepari et al. 2016). comprises three tribes: , , and whereas consists of only two tribes: and (Robertson et al. 2015)

Worldwide, nearly 6000 species spanning nearly 360 genera are known. Approximately 90 % of the species are predators of aphids, coccids, psyllids, aleyrodids, chrysomelid larvae, and mites, the remainder being herbivorous or mycetophagous (Inayatullah 1984, Majerus 1994, Obrycki and Kring 1998, Iperti and Bertand 2001, Vandenberg 2002, Hodek 2012).The are an important group of beetles from both an economic standpoint in their use as biological control agents and in their diversity and adaptation to a number of differing habitats (Michels 1987).

From Pakistan, Ahmad and Ghani (1966, 1968, 1970, 1973), Inayatullah and Siddiqui (1978, 1979, 1980), and Ali et al. (2012) worked on different species of the family ; Iablokoff-Khnzorian (1986) described a new species from Pakistan; Hashmi and Tashfeen (1992) studied the coccinellids housed in different institutions of Pakistan and reported 162 species, identifying the coccinellids deposited in the Natural History Museum, London, but with wrong synonymies. The present authors tried to trace this valuable collection of coccinellids in the present institutions in Karachi and other cities of Pakistan but found very few coccinellids. The authors also tried to correct the wrong synonymies and wrong identifications mentioned in the above-mentioned paper with the help of checklists and taxonomic papers available. Irshad (2001) listed 71 species of coccinellids in Pakistan; Rafi et al. (2005) gave a brief external morphology of predatory coccinellids of northern parts of Pakistan with special reference to their hosts, prey and localities, and listed 37 genera and 75 species belonging to different tribes of subfamilies , , , , and . All listed species are very common in Pakistan and represent a much less complete inventory than that of Hashmi and Tashfeen (1992). Otherwise, the description of genitalia was totally absent. Ali et al. (2012, 2013, 2014, 2015) conducted a systematic study from Sindh Province for the first time. They listed 29 coccinellids with four new records and four varieties of .

According to Ghouri 1960, Kazmi 1980, Hashmi et al. (1983), Ali and Munir 1984, Ghani 1985, Inayatullah 1984, Mohyuddin and Mahmood 1993, Buriro 1996, Jan et al. 2003, Aslam et al. 2004, Abbas et al. 2007, Solangi et al. 2007, Massod et al. 2008, Rafiq et al. 2008, Arif et al. 2009, Mari and Lohar 2010, Iqbal et al. 2008, Iqbal et al. 2011, and Masood 2011, the following viz., (Rondani), (Fabricius), Glover, Scopoli, Boyer de Fonscolombe, (Koch) (Fitch), (Monell), (Thomas), (Kaltenbach), (Linnaeus), (Sulzer), and (Das) (: ); (Lethierry)), (Ishida), (Bergevin and Zanon) (: ); (Gennadius), (Maskell), (Ashmead) and Corbett (: ); McGregor (: ), (Klein), and McG. (: ) are common pests of wheat, cotton, sugarcane, mango, mustard, vegetables, and fruits in Pakistan. Other works related with the taxonomy, morphology, diversity, distribution and ecology of different coccinellids include Rahman (1940), Ahmad (1969), Irshad (2001b), Khan et al. (2006), Rahatullah et al. (2010, 2011, 2012); Ali et al. (2012); Abbas et al. (2013), and Ashfaque et al. (2013). Ali (2012, 2013, 2014, 2015) was the first to report 29 coccinellid species from Sindh with a brief study on the taxonomy of the family and their role in the field of biological control of important agricultural crop pests such as aphids, mealybugs, scale insects, jassids, and whiteflies.

The coccinellid fauna of Sindh, Pakistan is insufficiently known, and no checklist exists. The goal of this paper is to contribute to the knowledge of diversity and distribution of ladybirds in Sindh as well as to present the first preliminary checklist of the species recorded previously in the territory of Sindh.

Materials and methods

Ladybird records presented in this paper were collected, identified, and confirmed during the last four years by the authors following the checklists, descriptions, and keys given by Chapin and Ahmad (1966), Pang and Gordon (1986), Poorani (2004), and Rafi et al. (2005), and with the help of the following website: NBAIR (2009). Ladybirds were also identified and confirmed by Dr. Claudio Canepari (Societa Entomologica Italiana), an authority on the family . Specimens were collected during field trips conducted in different parts of Sindh Province, and in reality represent random findings instead of systematic collecting. Beetles were collected in standard ways, including manual collecting, net sweeping, and using light traps. The terminologies for various taxonomic structures including genitalia and procedures used by Inayatullah and Siddiqui (1978) and Gordon (1985) were generally followed. The taxonomic structures, especially male and female genitalia, were preserved after illustration in microvials with glycerine and pinned with specimens.

Results

The coccinellids present in this checklist are classified on the basis of the new classification given by Seago et al. 2011, Robertson et al. 2015, and Canepari 2016. According to this classification all the coccinellids of the Sindh Province belong to the subfamily only. It includes nine species of the tribe , one species of the , one species of the tribe , five species of the , one species of the Tribe Mulsant, one species from Tribe , one species from the Tribe , six species of , one species of the Tribe , and three species of the Tribe . New records are (Hummel), Küster, Motschulsky, Marseul with four varieties of (Fabricius).

Subfamily Latreille, 1807

Tribe Latreille, 1807

Linnaeus, 1758

Linnaeus, 1758

Fig. 1

Figure 1.

Linnaeus.

General distribution.

India, Nepal, Sri Lanka, Pakistan, Palaearctic. North America (Poorani 2002).

Distribution in Sindh.

Tandojam, Larkana, Mirpur Khas, Thatta, Karachi (Sarwar 2009, Mahmood et al. 2011, Ali 2013, Fazal Ellahi et al. 2017).

Host plants and prey species in Sindh.

(L), (Kaltenbach), (Sulzer), (Glover), (Das), (Thomas), (Rondani) (: ); (Tinsley), (Ckll) (: ); (Dist), (Ishida) (: ); (Gennadius) (: ) on mustard, lucern, cabbage, cauliflower, potato, turnip, bottle gourd, eggplant, okra, wheat, cotton, sugarcane, and rose plants (Ali 2013).

Linnaeus, 1758

Fig. 2

Figure 2.

Linnaeus.

India, Pakistan. Palaearctic (Poorani 2002).

Karachi, Hyderabad, Tandojam, Mirpur Khas and Thatta (Sarwar 2009, Mahmood et al. 2011, Ali 2013, Fazal Ellahi et al. 2017).

(L.), (Kaltenbach), (Sulzer), (Glover), (Das), (Thomas), (Rondani) (: ); (Tinsley), (Ckll) (: ); (Dist), (Ishida) (: ); (Gennadius) (: ) on mustard, lucern, cabbage, cauliflower, potato, turnip, bottle gourd, brinjal, okra, wheat, cotton, sugarcane, and rose plants (Ali 2013).

Fabricius, 1781

Fig. 3

Figure 3.

Fabricius.

India, Nepal, Sri Lanka, Bangladesh, Indochina, Indonesia, Japan, Australia, New Zealand (Poorani 2002).

Hyderabad, Larkana, Mirpur Khas, and Thatta (Ali 2013).

(L.), (Kaltenbach), (Sulzer), (Glover), (Das), (Thomas), (Rondani) (: ); (Tinsley), (Ckll) (: ); (Dist), (Ishida) (: ); (Gennadius) (: ) on mustard, lucern, cabbage, cauliflower, potato, turnip, bottle gourd, brinjal, okra, wheat, cotton, sugarcane, and rose plants (Ali 2013).

Dejean, 1836

(Fabricius, 1781)

Fig. 4

Figure 4.

(Fabricius).

India, Bangladesh, Pakistan, Sri Lanka, Bhutan, Myanmar. Malaysia, Indonesia, Philippines, Vietnam, China, Japan, Australia (Poorani 2002).

Hyderabad, Larkana, Mirpur Khas, and Thatta (Sarwar 2009, Mahmood et al. 2011, Ali 2013, Balouchi and Swati 2014, Fazal Ellahi et al. 2017).

Koch, Glover, (L.), (Kaltenbach), (Sulzer), (Glover), (Das), (Thomas), (Rondani), (Fitch), Monell (: ); (Tinsley), (Ckll), Green (: ), (Green) (: ) Corbett, Ashby, Mask (Dist), (Ishida), Leth, Dist (: ); (Gennadius) (: ), Walk (: ), Comst (: ), Kuw (: ), Mog (: ) on mustard, lucern, cabbage, cauliflower, potato, turnip, bottle gourd, eggplant, okra, wheat, cotton, and rose plants (Ali 2013).

Comment.

Common. It is very difficult to compare this species with other taxa because of polymorphism. Six varieties of this species are reported from Pakistan.

(Goeze, 1777)

Fig. 5

Figure 5.

(Goeze).

Nepal, Pakistan, Afghanistan, Tibet, Mongolia, China, northern and eastern Africa, Palaearctic (Poorani 2002).

Hyderabad, Karachi, and Thatta (Lohar et al. 2012, Ali 2013).

(L.), (Kaltenbach), (Sulzer), (Glover), (Das), (Thomas), (Rondani) (: ); (Tinsley), (Ckll) (: ); (Dist), (Ishida) (: ); (Gennadius) (: ) on mustard, lucern, cabbage, cauliflower, potato, turnip, bottle gourd, brinjal, okra, wheat, cotton, and rose plants (Ali 2013).

(Mulsant, 1866)

Fig. 6

Figure 6.

(Mulsant).

India, Nepal, Pakistan, Myanmar, Indonesia (Poorani 2002).

Hyderabad, Mirpur Khas, Thatta and Karachi (Ali 2013).

Teth (: ) Comst (: ), Walk (: ) (Ali 2013).

Mulsant, 1866

Fig. 7

Figure 7.

Weise.

India, Bhutan, Pakistan, Nepal, Myanmar, Thailand, China (Poorani 2002).

Hyderabad, Mirpur Khas, Thatta, and Karachi (Ali 2013).

Host plants and Prey species in Sindh.

Koch, Glover, (L.), (Kaltenbach), (Sulzer), (Glover), (Das), (Rondani), (Fitch) (: ), Mask (Dist), (Ishida), Dist (: ), sp. (: ) on wheat, mustard, and cabbage (Ali 2013).

(Linnaeus, 1758)

Fig. 8

Figure 8.

(Linnaeus).

India, Pakistan, Bangladesh, Japan, China, Europe, North America (Poorani 2002).

Hyderabad and Karachi (Ali 2013).

Koch, Glover, (L.), (Kaltenbach), (Sulzer), (Glover), (Das) (: ), Mask (Dist), (Ishida), Dist (: ) (Ali 2013).

(Fabricius, 1781)

Fig. 9

Figure 9.

(Fabricius).

India, Pakistan, Nepal, Bhutan, China, Japan, Taiwan, introduced into North America (Poorani 2002).

Hyderabad and Karachi (Ali 2013).

Koch, Glover, (L), (Kaltenbach), (Sulzer), (Das), (Thomas), (Fitch), Monell, (Kirby), (Rondani) (: ), Leth, Pruthi (: ); (Gennadius) (: ), Mog (: ), spp. (: ) on mustard, lucern, cabbage, cauliflower, potato, turnip, bottle gourd, eggplant, okra, wheat, cotton, and rose plants (Ali 2013).

Tribe Savoiskaja, 1969

(Hummel, 1827)

Fig. 10

Figure 10.

(Hummel).

General distribution.

Pakistan, India, Central and West Asia, Afghanistan, Mediterranean region. North and Central Africa (Poorani 2002, Ali 2013).

Distribution in Sindh.

Hyderabad and Karachi (Ali 2013).

Host plants and prey species in Sindh.

Koch, Glover, (Sulzer), Kuw (: ) on wheat and mustard.

Comments.

Newly recorded from Pakistan.

Tribe Casey, 1899

(Mulsant, 1850)

Fig. 11

Figure 11.

(Mulsant).

India and Pakistan (Poorani 2002).

Hyderabad and Karachi (Ali 2013).

Prey in Sindh.

All the members of this genus are mycophagous (Ali 2013).

Tribe Costa, 1849

Leach, 1815b

(Fabricius, 1798)

Fig. 12

Figure 12.

(Fabricius).

Agalega, American Samoa, Burma, Brazil, Ghana, Guam, Hawaii, India, Indonesia, Kenya, Madagascar, Malaysia, Marshall Islands, New Caledonia, Nepal, Oman, Pakistan, Reunion Island, Seychelles, Solomon Islands, South Africa, Swaziland, Society Islands, Tanzania, Togo, Turkey and Zimbabwe (Nandwani and Joseph 2003, NBAII 2011, Omkar and Pervez 2003, Poorani 2002, Thomas and Blanchard 2014).

Tandojam, Hyderabad and Karachi (Ali 2013).

(Mask), (Coq), Newst, Sign, (Sign), Hall & Williams, spp, (Cooley), Comst, spp. (: ) (Ali 2013).

Erichson, 1843

Fig. 13

Figure 13.

(Erichson).

northwestern India, Pakistan, Palaearctic, Africa (Poorani 2002).

Tandojam, Mirpur Khas, Hyderabad, and Karachi (Ali, 2013).

Theobald, Fitch (: ), spp. (: ), (Ckll) (: ). It was recorded on trees and wild plants (Ali 2013).

Küster, 1848

Fig. 14

Figure 14.

Küster.

Pakistan, India, Spain, North Africa, Greece, Egypt, Syria, Palestine (Poorani 2002).

Karachi (Ali 2013).

spp. (: ). It was found on oak (Ali 2013).

Newly recorded from Pakistan.

(Mulsant, 1853)

Fig. 15

Figure 15.

(Mulsant).

India, Bhutan, Pakistan, Nepal (Poorani 2002).

Tandojam and Hyderabad (Ali 2013).

spp., (Cooley), Comst, spp. (: ) on wild trees, and shrubs (Ali 2103).

(Fabricius, 1798)

Fig. 16

Figure 16.

(Fabricius).

India, Pakistan, Bangladesh, Sri Lanka, Bhutan, Nepal (Poorani 2002).

Tandojam, Mirpur Khas, Hyderabad, and Karachi (Ali 2013).

Koch, Glover, (L.), (Kaltenbach), (Sulzer), (Das), (Thomas), (Fitch), Monell, (Kby), (Rondani) (: ); (Tinsley), (Ckll) (: ), (Green) (: ), (Dist), (Ishida) (: ); (Gennadius) (: ), Mog (: ), S.O & S (: ), (Mask), (Coq), Newst, Sign, (Sign), Hall & Williams, spp, (Cooley), Comst, spp. (: ) on mustard, lucern, cabbage, cauliflower, potato, turnip, bottle gourd, eggplant, okra, wheat, cotton, and rose plants (Ali 2013).

Tribe Mulsant, 1850, Genus Mulsant, 1850

Mulsant, 1850

Fig. 17

Figure 17.

Mulsant.

India, Pakistan, Thailand (Poorani 2002).

Karachi and Mirpur Khas (Ali 2013).

(Dougl) (: ). It was found on cotton and roses (Ali 2013).

Tribe Costa, 1849, Genus Chevrolat, 1836

Sicard, 1929

Fig. 18

Figure 18.

Sicard.

Pakistan and India (Poorani 2002).

Tandojam, Mirpur Khas, and Karachi (Ali 2013).

(Green), sp, (Tinsley), (Ckll) (: ), (Green) (: ). It was found on cotton, okra, and trees (Ali 2013).

Tribe Dobzhansky, 1924, Genus Weise, 1885b

(Mulsant, 1850)

Fig. 19

Figure 19.

(Mulsant).

India, Pakistan, Italy, Cyprus (Poorani 2002).

Tandojam, Hyderabad, Mirpur Khas and Karachi (Ali 2013).

sp. (: ), (B&P), (Klein), Mog (: ). It was collected from eggplant, okra, and some wild plants (Ali 2013).

Tribe Mulsant, 1846, Genus , Mulsant, 1850

Mulsant, 1850

Fig. 20

Figure 20.

Mulsant.

Pakistan, India, Bangladesh, Sri Lanka, Nepal, Myanmar, China, Asia Minor (Poorani 2002).

Tandojam, Mirpur Khas, Hyderabad, and Karachi (Ali 2013).

Koch, Glover, (L.), (Kaltenbach), (Sulzer), (Glover), (Das), (Thomas), (Fitch), Monell, (Kby), (Rondani) (: ); (Tinsley), (Ckll) (: ), (Green) (: ), (Dist), (Ishida) (: ); (Gennadius) (: ), Mog (: ), S.O & S (: ), (Mask), (Coq), Newst, Sign, (Sign), Hall & Williams, spp, (Cooley), Comst, spp. (: ) on mustard, lucern, cabbage, cauliflower, potato, turnip, bottle gourd, eggplant, okra, wheat, cotton and rose plants (Ali 2013).

Motschulsky, 1858

Fig. 21

Figure 21.

Motschulsky.

Pakistan, India, Bangladesh, Sri Lanka, Thailand, Taiwan. (Poorani 2002; Ali 2013).

Tandojam, Hyderabad, and Karachi (Ali 2013).

Koch, Glover, (L.), (Kaltenbach), (Sulzer), (Glover), (Das), (Thomas), (Fitch), Monell, (Kby), (Rondani) (: ); (Tinsley), (Ckll) (: ), (Green) (: ), (Dist), (Ishida) (: ); (Gennadius) (: ), Mog (: ) on mustard, lucern, cabbage, cauliflower, potato, turnip, bottle gourd, eggplant , okra, wheat, cotton, and rose plants (Ali 2013).

Comment.

Newly recorded from Pakistan.

Ayyar, 1925

Fig. 22

Figure 22.

Ayyar.

India, Pakistan, Bangladesh, Sri Lanka, Malaysia (Poorani 2002).

Tandojam, Hyderabad, and Karachi (Ali 2013).

Koch, Glover, (L.), (Kaltenbach), (Sulzer), (Glover), (Das), (Thomas), (Fitch), Monell, (Kby), (Rondani) (: ); (Tinsley), (Ckll) (: ), (Green) (: ), Mog (: ) on mustard, lucern, cabbage, cauliflower, potato, turnip, bottle gourd, eggplant, okra, wheat, cotton, and rose plants (Ali 2013).

Sicard, 1929

Fig. 23

Figure 23.

Sicard.

Pakistan, India, Bangladesh (Poorani 2002).

Tandojam, Hyderabad and Karachi (Ali 2013).

Koch, Glover, (L.), (Kaltenbach), (Sulzer), (Glover), (Das), (Thomas), (Fitch), Monell, (Kby), (Rondani) (: ); (Tinsley), (Ckll) (: ), (Green). It was found on eggplant, okra, cotton (Ali 2013).

Newly recorded from Pakistan.

(Marseul, 1868)

Fig. 24

Figure 24.

(Marseul).

Iran, Afghanistan, Pakistan (Ali 2013).

Hyderabad and Karachi (Ali 2013).

Koch, Glover, (L.), (Kaltenbach), (Sulzer), (Glover), (Das), (Thomas), (Fitch), Monell, (Kby), (Rondani) (: ) (Ali 2013).

Newly recorded from Pakistan.

(Sicard, 1929)

Fig. 25

Figure 25.

(Sicard).

India, Pakistan, China (Poorani 2002).

Tandojam, Mirpur Khas, Hyderabad and Karachi (Ali 2013).

Prey and host plant.

Koch, Glover, (Glover), (Das), Monell (: ); (Tinsley), (Ckll) (: ), (Green) (: ) on on eggplant, okra and cotton (Ali 2013).

Tribe Sasaji, 1967, Genus Ahmad, 1973

Ahmad, 1973

Fig. 26

Figure 26.

Ahmad.

Pakistan (Poorani 2002).

Karachi (Ali 2013).

(Mask), (Coq), Newst, (Sign), Hall & Williams, spp. (Cooley), Comst, spp. (: ) (Ali 2013).

Tribe Weise, 1901

(Mulsant), 1853

Fig. 27

Figure 27.

(Mulsant).

India, Pakistan, Brazil, and United States (Florida) (Poorani 2002, Thomas and Blanchard 2013).

Tandojam, Mirpur Khas, Hyderabad, and Karachi (Ali 2013).

Sign, (Sign), Hall & Williams, spp, (Cooley), Comst, spp. (: ), L, (Nietn) (: ) on wheat and mustard (Ali 2013).

Ahmad, 1970

Fig. 28

Figure 28.

Ahmad.

Pakistan, Thailand (Poorani 2002).

Karachi (Ali 2013).

spp., (Cooley), Comst, spp. (: ), L, (Nietn) (: ) on wheat and mustard (Ali 2013).

(Weise), 1900

Fig. 29

Figure 29.

(Weise).

India and Pakistan (Poorani 2002).

Karachi (Ali 2013).

spp. (Cooley), Comst, spp. (: ), L, (Nietn) (: ) on mustard and wheat (Ali 2013).

Discussion

Unfortunately, all the specimens were lost during the shifting of Vitoria Museum to National Museum at Karachi. From Pakistan very little taxonomic work has focussed especially on this important family of the order . Irshad (2001) listed 71 species of coccinellids from northern parts of Pakistan. Rafi et al. (2005) listed 37 genera and 75 species and described the only external morphology of predatory coccinellids mostly collected from northern parts of Pakistan with special reference with their hosts, prey, and localities.

Sindh Province has a rich insect fauna which have diversified into important cities like Karachi, Tandojam, Hyderabad, Larkana, Sukhur, and Mirpur Khas. Coccinellids fauna is still incompletely recorded from Sindh region and has been neglected in the past. All the research findings on coccinellids except Ali (2013) were documentary not taxonomic. No proper collections, identification procedures,or techniques have been used in Sindh to explore the hidden records of insects, including the coccinellid fauna. Ali (2013) worked more comprehensively on the systematics and distribution of ladybirds of Sindh Province with reference to their role in biological control programmes. He tried to highlight the importance of systematic study to make easy their identification as predators of mealybugs, aphids, jassids, whiteflies, and scale insects. This research work may be useful for the entomologists including research students of particularly the Sindh region, but also of Pakistan and other Oriental regions. The geographical distribution and synonyms used in this study for all systematically treated specimens were cited from the findings of Hashmi and Tashfeen (1992).

The present investigation continues the research carried by Ali (2013), and gives a preliminary checklist of ladybirds from Sindh consisting of only one subfamily, ten tribes, 21 genera, and 29 species including four new records: (Hummel), Küster, Motschulsky, Marseul and four varieties of (Fabricius). All these coccinellids from Pakistan are now placed into the subfamily and the subfamily according to the recent classification studies. The coccinellid specimens were deposited in the Natural History Museum, Department of Zoology, University of Karachi, Karachi, Pakistan.